MAGNOLIOPSIDA
Brongn.

Maximum likelihood (ML)
majority-rule consensus tree of Magnoliopsida
(Pan-Angiospermae) based on DNA sequence data
(Soltis & al. 2011, slightly modified).
Amborella, Nymphaeales
and Schisandrales
being successive sister-groups to all other angiosperms
had more than 80% bootstrap (BS) support in the 17-gene
analysis by Soltis & al. (2011). The position of
Amborella as sister to all other angiosperms is
highly supported by complete plastid genome sequence
analyses (Kim, Yoo & al. 2004; Moore & al. 2007;
Soltis & al. 2011; etc.). The sister-group
relationship [Chloranthaceae+Magnoliidae]
had a BS support of 85%. The clades [Magnoliales+Laurales]
and [Canellales+Piperales]
each had a BS support of 100%. The clade comprising
Liliidae, Ceratophyllum and
Tricolpatae was supported by 86%, whereas the
support of Ceratophyllum as sister to
Tricolpatae was only 68%. The BS support for
Sabiaceae
as sister to the remaining Tricolpatae (a
trichotomy in this tree) was likewise relatively low
(59%). Sabiaceae
are sometimes recovered as sister to Proteales,
yet with weak to moderate support (Qiu & al. 2006;
Moore & al. 2008; Burleigh & al. 2009; Moore
& al. 2011; Soltis & al. 2011). Gunnerales
were sister to the Pentapetalae with a BS support
of 99%. Ranunculales
were as usual sister to the remaining Tricolpatae
(BS support 100%). The positions of Didymelales
and
Trochodendrales as successive sister-groups to
Gunneridae had a BS support of 98% and 100%,
respectively (Moore & al. 2010; Soltis & al.
2011). Gunnerales
were sister to the remaining angiosperms, the
Pentapetalae, with a support of 100%.
Superasteridae (Santalales
to Asteridae) and Superrosidae (Saxifragales
and Rosidae) were supported by 87% and 100%,
respectively. In some other analyses
Berberidopsidales were sister to
Asteridae, and Caryophyllales
were sister to these two groups. The position of
Dilleniaceae
as sister to Superasteridae was supported by 97%
in Soltis & al. (2011). In some other analyses they
were recovered as sister to, i.a., the remaining
Pentapetalae, or to the clade
[Superasteridae+Superrosidae] or to
Superrosidae, although with fairly low support
(Moore & al. 2010). The maximum parsimony (MP)
consensus tree was largely identical to the ML tree,
although Ceratophyllum was sister to
Liliidae and Dilleniaceae
were sister to Caryophyllales.
– Extant angiosperms began to diversify in the
mid-Jurassic, c. 170 Mya, according to unconstrained
penalized likelihood analyses (Moore & al. 2007), and
the five major mesangiosperm lineages diversified fairly
rapidly during the earliest Cretaceous. The initial
divergence of these five lineages was dated to
143.8+4.8 Mya, and the divergence
of Chloranthus and Magnoliidae was dated to
140.3+4.8 Mya. The origins of the
extant crown groups of Magnoliidae,
Liliidae, and Tricolpatae were dated to
branching points somewhat later in the Cretaceous:
130.1+4.4 Mya for
Magnoliidae, 128.9+4.9 Mya
for Liliidae, and 124.8+6.3 Mya for Tricolpatae. Divergence
times and standard errors (in parentheses) in Mya for
deep-level angiosperm nodes as estimated by penalized
likelihood analyses were as follows: angiosperms 169.7
(3.46) – Nymphaeales+Illicium+Mesangiospermae
163.5 (2.63) – Illicium+Mesangiospermae
154.8 (2.53) – Mesangiospermae 143.9 (2.67) –
Chloranthus+Magnoliidae 140.4 (2.54) –
Magnoliidae 130.3 (2.20) –
Liliidae+Ceratophyllum+Tricolpatae
143.1 (3.18) – Liliidae 129.1 (2.69) –
Ceratophyllum+Tricolpatae 141.4 (2.97) –
Tricolpatae 124.9 (3.43).

Flower Flower
bisexual or unisexual. Symmetry actinomorphic, bisymmetrical,
zygomorphic or asymmetrical. Pedicel present or absent, usually
provided with one or two floral prophylls (bracteoles). Floral
parts spirally arranged or whorled in one or more series. Floral
parts usually present in stable (sometimes unstable) numbers.
Perianth differentiated into sepals and petals or
undifferentiated. Tepals usually centripetally developing, with
usually one or three traces, free or more or less connate,
persistent or caducous. Outer tepals (sepals) enclosing or not
enclosing remainder of floral bud. Floral parts when whorled
usually trimerous, tetramerous or pentamerous. Floral nectaries
of various origin present or absent.

Androecium
Stamens usually centripetally (sometimes centrifugally)
developing. Each stamen usually supported by one trace. Stamen
usually differentiated into filament and anther (microsporangia
sometimes embedded in distal part of stamen). Filament
band-shaped or terete, usually narrow (sometimes wide and stout).
Anther usually dithecal (microsporangia organized in two groups
each with two sporangia; sometimes monothecal etc.),
tetrasporangiate (sometimes disporangiate or polysporangiate),
introrse, latrorse or extrorse. Microsporangia with at least
outer secondary parietal cells dividing. Thecae usually dehiscing
longitudinally (longicidally) by action of hypodermal endothecium
(sometimes poricidally, valvicidally etc.). Endothecial cells
usually elongated at right angles to longitudinal axis of anther.
Tapetum usually secretory (glandular), with binucleate (sometimes
uninucleate or multinucleate) cells (sometimes
amoeboid-periplasmodial).

Gynoecium
Carpels usually several or numerous, usually more or less connate
(sometimes free). Carpels plicate or ascidiate, postgenitally
usually fused (sometimes occluded by secretion). Compitum usually
present. Carpellary distal-adaxial pollen-receptive part usually
papillate or non-papillate, Dry or Wet (secretory) type stigma
(receptive area sometimes present along free carpellary margins).
Pollen grains deposited on receptive surface. Stigmatic surface
also aiding in development of pollen tubes. Stylar part of
gynoecium present or absent (stigma sessile), often hollow (with
central canal).

Ovule
Placentation of different types (axile, parietal, laminar etc.).
Ovules usually anatropous, bitegmic or unitegmic and
crassinucellar or tenuinucellar. Micropyle endostomal, bistomal
or exostomal. Each integument one or several cell layers thick.
Inner integument dermal or subdermal in origin. Parietal tissue
present (ovule crassinucellar) or absent (ovule tenuinucellar).
Megasporocyte usually single (archespore sometimes
multicellular), hypodermal, present in centre of ovule.
Cytoplasmically dense zone developing between megasporocyte
nucleus in centre of cell and chalazal cell wall, this dense zone
persisting through megasporogenesis. Megasporogenesis resulting
in usually linear tetrad. Functional megaspore without
sporopollenin and cuticle and usually chalazal. Megagametophyte
usually monosporic and developing from chalazal cell. Meiosis I
resulting in a dyad of two uninucleate cells divided by
transverse cell wall. Meiosis II yielding a usually linear tetrad
of megaspore cells, of which chalazal cell becomes megaspore and
remaining three megaspores degenerating prior to initiation of
megagametogenesis. Large central nucleus of functional megaspore
surrounded by vacuole. Two nuclei migrating to opposite poles of
cell after first mitosis. Two nuclei present at each pole after
second mitosis, nuclei at micropylar pole becoming fusiform. Four
nuclei present at each pole after third mitosis, cytokinesis now
taking place. Resulting megagametophyte 8-nucleate and
septacellular. Three cells at micropylar end becoming egg
apparatus consisting of usually two synergids and one egg cell.
Each synergid often containing a cuneate filiform apparatus,
usually a small number of plastids and in general with thicker
wall than egg cell. Three cells at chalazal end becoming
antipodal cells, usually containing numerous plastids, and in
many cases proliferating (dividing). Nuclei of these cells more
or less fusiform (torpedo-shaped) and each with distinct
nucleolus. Remaining two nuclei, polar nuclei, of seventh cell,
central cell, moving to centre of megagametophyte. Here they are
situated in a parietal band of cytoplasm. Female gametangia
(archegonia) absent. Fertilization taking place some time between
one day and one year following pollination. Fertilization double,
i.e. one male gamete fusing with egg cell and second male gamete
with central cell containing two free or fused polar nuclei
(polar nuclei fusing in centre of central cell either immediately
prior to or during fertilization process and subsequently moving
into position adjacent to egg cell with its terminal nucleus).
Triploid cell resulting from fertilization of diploid central
cell usually developing into endosperm. Endosperm development
cellular, helobial or nuclear. Endosperm nuclei triploid.

Seeds Seed coat
consisting of one or several layers developed from integument(s).
Endosperm sparse to copious, oily and/or proteinaceous and/or
starchy (occasionally absent). Embryo ab initio cellular.
Cotyledons usually two (sometimes one, rarely three or four),
each usually provided with three vascular bundles (when one
cotyledon, then usually with two main vascular bundles). Plumule
usually terminal. Seedling with sympodial growth. Germination
usually phanerocotyl (sometimes cryptocotyl).

Cytology and
genes A genes are found only in angiosperms. A
duplication event took place in the ancestor of angiosperms,
which resulted in a D orthologue, usually expressed only in the
ovules, and a C orthologue, only occasionally expressed in
ovules, but in carpels and stamens as well.

Nuclear gene euAP3 in
angiosperms consisting of duplicated copy of gene
paleoAP3 with 8 bp insertion causing a frame-shift
mutation. APETALA3 and similar nuclear genes and
PISTILLATA are paralogous B-class genes. B-function
MADS-box genes are extremely important for the floral
development.

The exon 5’ in the
PI-homologues has a size of 42 base pairs in the
basalmost clades Amborella and Nymphaeales.
Illicium (Schisandrales)
and all younger clades has a deletion of 12 bp in this exon 5’
resulting in a length of 30 bp.

- Fossilized angiosperm leaves
occur in Aptian and younger layers. A peculiar leaf fossil is the
Aptian to Albian Trifurcatia flabellata, which is
connected to the fossil genus Klitzschophyllites. These
leaves are thick, circular in outline and with serrate margins.
The venation is flabellate with more than 20 primary and
secondary veins terminating at or between the leaf teeth.
Gland-like structures are present along the leaf margins.

- Small male flowers from the
Late Barremian to the Aptian (Early Cretaceous) of Portugal, with
ten to 15 stamens having wide flat filaments and lateral thecae
and trichotomocolpate pollen grains, are in some way similar to
Amborella trichopoda, although the anthers were extrorse
instead of introrse and the pollen surface was
verrucate-rugulate.

- The Early Cretaceous (Early to
Late Aptian, the Liaoning Province in northeastern China)
probably limnic species of Archaefructus were herbaceous
with multiple times divided leaves and leaflets. They had naked
unisexual terminal reproductive organs usually arising in pairs,
with female and male parts separate on the elongating axis.
Bracts and perianth seem to have been absent. The seed-bearing
carpel-like organs (possibly developing into follicles) were
elongated and slightly stipitate and the stamen-like organs were
present two to four together on a common stipe. The reproductive
organ has been interpreted as a single bisexual flower or as an
inflorescence consisting of numerous unisexual units.
Archaefructaceae were recovered as sister to all other
angiosperms in a combined morphological and 3-gene-analysis by
Sun & al. (2002). Archaefructaceae comprise the two
species Archaefructus liaoningensis Sun, Dilcher, Ji
& Zhou and A. sinensis Sun, Dilcher, Ji &
Nixon.

- Cronquistiflora and
Detrusandra from the Turonian (93,5–89 Mya) in New
Jersey had numerous spiral carpels and other floral parts.

- Caloda delevoryana,
from Late Albian to Early Cenomanian (mid-Cretaceous) strata of
the central United States, is represented by elongate
infructescences bearing alternately arranged lateral branches
each ending in a receptacle with numerous free stipitate
carpels.

- The floral fossil
Carpestella lacunata, from the Early to Middle Albian
(Early Cretaceous) of Virginia, may have been related to extant
basalmost angiosperms. The fossil consists mainly of a syncarpous
gynoecium with 13 carpels covered by spiral scars of detached
perianth and androecium.

- Caspiocarpus
paniculiger is represented by a single shoot from the
mid-Albian of Kazakhstan, having opposite palmately veined leaves
and paniculate reproductive axes bearing follicle-like
fruits.

- Cretovarium japonicum
from the Coniacian to Campanian (Late Cretaceous) of Hokkaido
(Japan) has perianth-like structures surrounding a trilocular
inferior ovary with axile placentation (two separate placentae in
each locule).

- Hidakanthus shiinae
and Protomonimia kasai-nakajhongii are multicarpellate
fruit structures from the Coniacian to Santonian (Late
Cretaceous) of Hokkaido (Japan). Hidakanthus has c. 55
sessile carpels with oil cells and Protomonimia c. 170
or stipitate carpels on a concave receptacle. The seeds of
Protomonimia are exotestal.

- Lesqueria elocata
represents elongate infructescences from the Late Albian to Early
Cenomanian (mid-Cretaceous) of Kansas and northern Texas. The
gynoecium was apocarpous and multicarpellate, and bore up to c.
150 helically arranged laminar appendages and up to c. 250
stalked follicles.

- Xingxueina
heilongjiangensis is an Aptian spicate inflorescence from
the Heilongjiang Province in northeastern China. The proposed
floral units are situated in an elongated helix. The monocolpate
pollen grains have a reticulate exine.

- Zlatkocarpus
brnikensis and Z. pragensis resemble the
Chloranthaceae.
They have spicate inflorescences with helically arranged floral
units containing a single carpel subtended by an adnate bract and
probably developed into a berry with resin bodies (possibly
ethereal oil cells) in the pericarp.

- A number of flowers have been
described from Cretaceous strata in New Jersey and Portugal.
Mabelia (Turonian, Late Cretaceous) and
Nuhliantha (Late Santonian, Late Cretaceous) were
trimerous and unisexual, with six tepals and three extrorse
stamens containing monocolpate (monosulcate) or trichotomocolpate
pollen grains. With the exception of a pistillodium in
Nuhliantha no female organs are known. The floral
morphology suggests a monocotyledonous affinity.
Microvictoria (Turonian) consists of bisexual
pedicellate flowers bearing numerous tepals (or bracts?),
flattened staminodia and stamens and carpels. They are similar to
flowers in Nymphaeaceae,
although this relationship may be questioned.

- Numerous fossilized fruits and
seeds occur in Cretaceous layers. The Early Cretaceous
Anacostia represents small single-seeded berries with
exotestal anatropous seeds. Trichotomocolpate pollen grains with
reticulate tectum are often associated with these fruits. The
flowers seem to have been apocarpous with several or many
carpels. Couperites likewise comprises single-seeded
berries with exotestal anatropous seeds, often found together
with monocolpate pollen grains with reticulate sexine similar to
the Clavatipollenites pollen type.

- Angiosperm pollen grains are
frequent in Cretaceous beds. The Afropollis form genus
includes spheroidal, acolumellate coarsely reticulate grains,
usually with a granular infratectum. They may be zonacolpate,
monocolpate or inaperturate and either isopolar or heteropolar.
Afropollis occurs in Early Cretaceous layers from the
Barremian to the Cenomanian. The angiospermous origin of
Afropollis has been questioned, i.a. due to the presence
of a thick laminar endexine unknown among extant flowering
plants. The similar Schrankipollis form genus from the
Early Cretacous represents zonacolpate, loosely reticulate pollen
grains with columellate infratectum.

- Clavatipollenites
comprises monocolpate pollen grains with a reticulate exine,
finely verrucate colpus membrane and indistinct colpus margins.
Many Clavatipollenites grains have been assigned to
Chloranthaceae,
and to Ascarina in particular, although the form genus
Clavatipollenites certainly represents several different
early angiosperm clades.

- Retimonocolpites
dividuus is an Early Cenomanian monocolpate pollen with a
reticulate exine and an aperture encircling most of the grain.
Brenneripollis represents monocolpate pollen grains with
irregularly reticulate exine and columellate infratectum, whereas
the similar Pennipollis has acolumellate
infratectum.

- Liliacidites is
monocolpate or trichotomocolpate and has a graded reticulum with
the small lumina concentrated in the equatorial area. This Early
Cretaceous to Early Cenozoic type resembles pollen grains of
extant monocotyledons. Similipollis, also with possible
monocotyledonous affinities, has the small lumina of the
reticulum concentrated in the polar area.

- The Barremian to Cenomanian
Stellatopollis comprises monocolpate pollen grains with
columellate infratectum and reticulate exine beset with clavate
supratectal elements which are borne in a stellate pattern. The
Albian Transitoripollis pollen type is monocolpate and
has continuous verrucate to microechinate tectum and granular
infratectum. The Barremian to Aptian Tucanopollis is
similar to Transitoripollis, but the colpus is sometimes
nearly circular in outline. The large Lethomasites
pollen type is also monocolpate and tectate with granular
infratectum, although the tectum is perforate.

Systematics The
main clades of flowering plants are briefly presented below. The
potential synapomorphies are mainly adopted from Peter F.
Stevens, “The Angiosperm Phylogeny Website”, version 9 (June
2008, updated in July 2012). More comprehensive descriptions are
given for Magnoliidae (the magnolids), Liliidae
(the monocots), Asteridae (the asterids), and
Rosidae (the rosids).

Androecium
Stamens (one or) two to c. 20 to more than 200, laminar
(foliaceous), spiral or whorled, not differentiated into filament
and anther, with separate microsporangia embedded in distal part
(adaxially, laterally, abaxially or apically), or differentiated
into filament and anther. Filaments when present usually free
from each other (sometimes partially or entirely connate;
occasionally adnate to pistil into synandrium or gynostemium),
usually free from tepals, sometimes with basal nectariferous
glands. Anthers when present usually basifixed, non-versatile,
usually free (rarely adnate to style), usually tetrasporangiate
(sometimes disporangiate), sometimes with transversely septate
thecae, extrorse, latrorse or introrse, longicidal (dehiscing by
longitudinal slits) or valvicidal (dehiscing by valves),
sometimes connate into synandrium; or microsporangia four,
usually adaxial or lateral (sometimes abaxial), usually introrse
or latrorse (sometimes extrorse), longicidal (dehiscing by
longitudinal slits) or valvicidal (dehiscing by valves). Tapetum
secretory or amoeboid-periplasmodial. Staminodia extrastaminal,
intrastaminal, or absent.

Gynoecium
Carpels usually ten to more than 50 (sometimes one or few),
spiral or whorled, free or more or less connate (sometimes
paracarpous); carpel plicate to conduplicate (sometimes basally
ascidiate and not differentiated into ovary and style), usually
postgenitally incompletely or entirely occluded by fusion and/or
secretion, with secretory canal, often open and filled by
secretions, or without canal. Carpels often not differentiated
into ovary, style and stigma. Ovary usually superior (sometimes
inferior, rarely semi-inferior), unilocular to 20-locular (or
more). Stylodium or style single, terminal, usually simple
(occasionally lobate), or stylodia lateral to gynobasic, or
absent (pollen tube transmitting tissue well developed). Stigma
capitate or lobate, terminal or decurrent, papillate or
non-papillate, Dry or Wet type. Nectar sometimes secreted from
exposed carpel surfaces. Pistillodium usually absent (male
flowers sometimes with pistillodium).

Fruit A usually
fleshy (sometimes leathery or more or less woody), dehiscent or
indehiscent, apocarpous follicular fruit or a multifolliculus, or
a dry or fleshy syncarp, a loculicidal (and occasionally
septicidal) capsule, or a drupe (sometimes a single-seeded berry
or an assemblage of achenes, berries, drupelets, dry follicles,
samaras, etc.).

Seeds Perisperm
usually not developed (in Piperales
usually copious, starchy). Endosperm copious (to scarce), oily
(occasionally also with compound starch grains), or absent.
Embryo straight or slightly curved, more or less differentiated
or undifferentiated, without chlorophyll. Cotyledons usually
two.

Fossils Examples
of early fossils not assigned to any particular magnoliid clade
are as follows.

- Araripia florifera,
from Upper Aptian to Lower Albian of Brazil, is represented by a
flowering shoot with decussate trilobate leaves. The tepals and
bracts are spirally inserted on a cupular receptacle. It has not
been possible to assign this fossil to a particular clade of the
Magnoliidae.

- Detrusandra mystagoga,
from the Turonian (Late Cretaceous) of New Jersey, is another
uplaced magnoliid fossil comprising pedicellate flowers with
cup-shaped receptacle, on which bracts and tepals are spirally
inserted. The numerous stamens are situated on the inner upper
part of the receptacle. The four microsporangia are adaxial on
each stamen. The pollen grains are monocolpate with a reticulate
exine. The five carpels are plicate and free and the stigmas are
bilobate. Ovules are numerous and arranged in two ventral
rows.

- Cronquistiflora
sayrevillensis is a Turonian floral fossil from New Jersey.
It resembles the above two fossils, having spirally arranged
bracts and tepals, but the receptacular cup is shallow. The
numerous free carpels are spirally inserted and terminating in a
peltate stigma. The ovules are interpreted as orthotropous,
bitegmic and with an endostomal micropyle.

- Canrightia resinifera,
from the Aptian to Early Albian of Portugal, comprises fossilized
flowers, fruits and seeds. The tepals are arranged in one whorl
and connate, forming a hypanthium. The pollen grains are
monocolpate with a reticulate exine and columellate infratectum.
The two to five carpels are unilocular, connate and adnate to the
tepals. The single ovule is orthotropous, endotestal-endotegmic
and has a well-developed endothelium (also present in the extant
Lactoris fernandeziana). Resin bodies are frequent on
the ovary walls, indicating the presence of oil cells. The fruit
was probably a berry.

Systematics
Cuticular wax crystalloids as transversely ridged rodlets
(Aristolochia type) are of high systematic significance
characterizing Magnoliales,
Laurales and
Piperales.
Sporadically, they also occur in various other taxa. Chemical
analyses show that transversely ridged rodlets clearly differ in
their composition. Waxes of one group are characterized by
ketones, whereas a second group completely lacks ketones and is
dominated by alkanes. Hentriacontan-16-one (palmitone) was found
to be characteristic for transversely ridged rodlets in
Aristolochia, Laurus, and Paeonia.
Transversely ridged rodlets or related crystals grow from total
waxes of all species but never crystallize from individual
compounds such as alkanes or palmitone. Transversely ridged
crystals are formed by self-assembly based on a slow
crystallization process and the presence of additives.

Androecium
Stamens (2–)3(–6)+(2–)3(–6) (sometimes one or three, rarely two,
five, 6+3, 6+4 or up to more than 1.000), usually as many as
tepals, usually antesepalous (sometimes antepetalous), whorled.
Staminal primordia often associated and/or stamens vascularized
from tepal trace. Anther and filament sharply distinguished.
Filaments free from each other or more or less connate (rarely
connate into synandrium), free from or adnate to tepals
(epitepalous; rarely to style). Anthers usually dorsifixed,
basifixed or subbasifixed (sometimes centrifixed), versatile or
non-versatile, usually tetrasporangiate (rarely disporangiate or
trisporangiate), introrse, latrorse or extrorse, usually
longicidal (dehiscing by longitudinal slits; sometimes poricidal,
dehiscing by one or two apical or subapical pores, or transverse
slits). Endothecium developing from outer secondary parietal cell
layer; inner secondary parietal cell layer dividing. Tapetum
usually secretory (sometimes amoeboid-periplasmodial), with
uninucleate to quadrinucleate cells. Staminodia present (rarely
petaloid) or absent (female flowers often with staminodia).

Fruit Usually a
loculicidal capsule (rarely septicidal, septifragal, poricidal,
ventricidal, irregularly dehiscent or indehiscent), a berry, nut
or drupe (sometimes a nut-like caryopsis, follicle, samara or
schizocarp, or an assemblage of achenes, drupelets or berrylets
or a multifolliculus).

Seeds Exotesta
usually with thin phytomelan layer on epidermal cell walls.
Perisperm usually not developed (sometimes well developed, with
lipids and proteins or compound starch grains). Endosperm copious
to sparse, often with starch (with simple or compound starch
grains), and/or lipids, aleurone and hemicellulose, or absent.
Chalazosperm developed or absent. Embryo straight to curved, well
or poorly differentiated, sometimes covered with discoid or
conical embryostega, testal operculum and surrounded by
micropylar collar, with or without chlorophyll. Cotyledon one
(rarely with rudimentary additional cotyledon), terminal,
sometimes photosynthesizing, with closed sheath, usually
unifacial (hyperphyllar; sometimes bifacial), assimilating and
haustorial, usually with two main vascular bundles. Plumule
lateral. Cotyledon hyperphyll elongate or compact, dorsiventrally
flattened, assimilating or not assimilating, sometimes modified
into haustorium or nutrient-storing organ. Hypocotyl internode
short to long (sometimes modified into nutrient-storing organ),
or absent. Mesocotyl present or absent. Coleoptile present
(sometimes modified into plumule envelope), with or without
lamina, or absent. Collar rhizoids or collar roots sometimes
present. Radicula unbranched, usually poorly developed,
contractile, persistent or ephemeral (rarely absent). First leaf
usually orientated at 180o to plane of cotyledon (in
most angiosperms orientated at 90o to plane of
cotyledons).

Fossils
Monocotyledon fossils are often difficult to distinguish from
other basal angiosperm groups. However, numerous fossils more or
less similar to extant Liliidae have been described
during the last decades. Many of these have not been assigned to
any particular extant clade.

- The oldest known fossil
Liliidae are 120–110 My old and resemble
Pothooideae (Araceae).

- Acaciaephyllum from
the Potomac Group of eastern North America represents herbaceous
plants with sheathing leaf bases and an acrodromous reticulate
venation. The taxonomic affiliation is highly questioned,
although they have been assigned to the monocotyledon stem group
(Doyle 1973, etc.).

- A number of fossilized leaves
and stems of monocotyledons have been found in Turonian layers in
Israel and in the Maastrichtian Deccan Intertrappen Beds of
India. These include Geonomites, Limnobiophyllum
dentatum, Plumafolium bipartitum, Pontederites
eichhornioides, Potamogetophyllum mite, Quturea
fimbriata, Typhacites negevensis, Aerophyllites
intertrappea, and Aerorhizos harrissii.

- Spinizonocolpites is a
Late Cretaceous pollen fossil strongly resembling the extant
Nypa (Arecaceae).
Early Cretaceous pollen types which have been referred to
monocotyledons due to their characteristic monocot morphology
include the sometimes frequently occurring Liliacidites
and Similipollis.

- Shuklanthus superbum
is a racemose inflorescence found in the Maastrichtian layers of
the Indian Deccan Intertrappean Beds, whereas Viracarpon
from the same layers represents an infructescence that may
actually belong to the same species. The unisexual flowers are
trimerous with six tepals and six uniovulate carpels. The fruits
consist of single-seeded drupelets.

- Deccananthus savitrii
from the Deccan Intertrappean Beds of India is a trimerous flower
with six tepals and six stamens. The pollen grains are
trichotomosulcate and the ovary is trilocular.

- Eriospermocormus
indicus is a fossilized corm from the Deccan Intertrappean
Beds. It is somewhat similar to the Eriospermum
(Ruscaceae),
but its systematic affiliation is uncertain.

SystematicsAcorus is sister to the remaining monocots and Alismatales
successive sister-group to the remainder.

A widely accepted hypothesis is
that Liliidae have evolved from helophytic (or even
aquatic) ancestors. Numerous adventitious roots replacing an
ephemeral main root (instead of a single tap-root), sympodial
growth, atactostele (vascular bundles scattered in stem), absence
from normal secondary lateral growth, and usually linear leaves
lacking normal lamina are characteristics of the monocots which
have been explained through this hypothesis. Moreover, most
members of the two basal monocot clades, Acorus and
Alismatales,
are helophytes or aquatic.

Reticulately veined pseudolamina
and baccate fruits – probable adaptations to forest habitats –
have evolved in parallel in many monocotyledon clades. According
to Givnish & al. (2005), baccate or drupaceous fruits have
evolved 21 times and reticulodromous venation perhaps between 25
and 30 times during the evolution of Liliidae.

Phylogeny of Liliidae based on
DNA sequence data (Tamura & al. 2004; Chase & al.
2006; Graham & al. 2006; Soltis & al. 2011).
Acorus and Alismatales
are supported by 100% (bootstrap-value) as successive
sister-groups to the remaining Liliidae. The clade
[Pandanales+Taccales]
also has very high support. Liliales
and Iridales
are successive sisters to the remainder, the Commelinidae
(a clade bootstrap support of 100%)

Potential synapomorphy:
Ethereal oils absent. – Ceratophyllum is sister to
Tricolpatae in the maximum-likelihood tree of Soltis
& al. (2011), but recovered as sister-group to
Liliidae in the maximum-parsimony tree of the same
study.

Ceratophyllum has a
large number of autapomorphies, in part due to their highly
specialized aquatic lifestyle. Roots, vessels, stomata and
cuticular waxes are absent and the perianth is reduced. Even
their pollen morphology – inaperturate (to indistinctly
monocolpate) and with very reduced exine – may be a result of
adaptation to an aquatic environment. The microsporogenesis is
successive (like in monocots) in some species and simultaneous
(like in most eudicots) in others. Further investigations of the
pollen development in Ceratophyllum are certainly
critical to our understanding of pollen character optimization
among Tricolpatae.

Ceratophyllum
share many features with the majority of Liliidae,
including ephemeral primary root, closed stem vascular bundles,
absence of interfascicular cambium, absence of vessels in stem
and leaves, perianth (if present) trimerous, and successive
microsporogenesis. On the other hand, it seems to be very
difficult to find morphological synapomorphies for the clade
[Ceratophyllum+Tricolpatae].

Fossils The
oldest known fossil tricolpate pollen grains have been found in
Late Barremian to Early Aptian strata in England, Portugal,
Israel, Egypt, tropical West Africa, and eastern North America.
The exine is finely to coarsely reticulate or striate, with a
columellate infratectum. Examples of early fossils not assigned
to any particular eudicot clade are as follows.

- Sinocarpus decussatus
comprises parts of infructescences and leaves from the Aptian of
China. The decussate leaves are provided with chloranthoid teeth
and the fruits are formed by three or four whorled and partially
connate carpels.

- Hyrcantha
karatscheensis is represented by reproductive axes and
fruits from the mid-Albian of Kazakhstan. The gynoecium is
composed of three to five free carpels.

- Ternariocarpites
floribundus is an infructescence with free carpels from the
Albian of the Russian Far East. The fruitlets are follicular and
the five tepals are persistent.

- Ranunculaecarpus
quinquecarpellatus from the Albian of East Siberia consists
of an apocarpous fruit with five follicular carpels. The
fossilized bicarpellate syncarpous fruit of Araliaecarpum
kolymense emanates from the same Siberian locality.

- The Cenomanian flower
Callicrypta chlamydea from eastern Siberia has a
perianth consisting of three whorls, stamens/staminodia and six
free carpels.

- Cathiaria zhilinii is
known from several localities from eastern Europe to Japan. It
comprises fruiting structures with monocarpellate single-seeded
fruits from the Cenomanian to the Coniacian.

- Numerous follicular fruits
(Agapitocarpus emisxus, Chontrocarpus
pachytoichus, Maiandrocarpus moirasmenus,
Malliocarpus batrachoides, Mitocarpus elegans,
Xylocarpus rhitidodes, Zeugarocarpus) have been
found in Late Santonian to Early Campanian layers of Sweden. The
different fossil species are relatively similar to each other.
The gynoecium is apocarpous or monocarpellate, the carpels are
plicate and the multiple ovules, when known, are anatropous and
bitegmic. Traces of tepals are absent.

Fossils In the
Late Albian to the Early Cenomanian of Nebraska, there are
unambiguous fossils of pentamerous heterochlamydeous flowers
(with differentiated calyx and corolla) which are assignable to
the Gunneridae.

Systematics
Several other gene duplications seem to have taken place in the
ancestors of either Gunneridae or Pentapetalae
(or sometimes even earlier), i.a. duplication of nuclear floral
regulatory genes AP1/FUL or FUL-like gene
(yielding euAP1, euFUL and AGL79);
duplication of nuclear gene RPB2; duplication of
AG-like C-class gene (yielding PLE and
euAG paralogs); duplication of nuclear genes
AGL2/3/4 (yielding SEP1 and FBP6) and
AGL1/2/3, etc. (see, i.a., Kramer & Zimmer 2006;
Kramer & al. 2004; Kramer & al. 2006). The knowledge of
many of these duplications is insufficient for many critical
clades (Proteales,
Sabiaceae,
Trochodendrales,
Didymelales,
Gunnerales,
Dilleniaceae,
Santalales,
Berberidopsidales,
etc.). Consequently, it is still impossible to optimize them
convincingly on the tree.

Since Gunnerales
are sister to Pentapetalae, detailed knowledge of floral
development in Gunnera and Myrothamnus is
important for our interpretation of floral characters in the
crown group of Tricolpatae. The flowers of Gunnerales
are strongly adapted to wind pollination, a fact that makes it
even more difficult to draw conclusions on homologies.
Furthermore, the organization of the androecial and perianth
whorls are more similar to basal Tricolpatae than to
Pentapetalae.

Potential synapomorphies:
Root apical meristem closed. Flowers pentamerous, with whorled
floral parts. Calyx/sepals and corolla/petals distinct. Sepals
enclosing flower in bud (sepals and petals encircling floral
axis). Sepals with three or more traces. Petals with one trace.
Nectariferous disc present. Stamens twice the number of
sepals/petals (sometimes numerous, but then usually fasciculate),
developing internally/adaxially to corolla whorl and successively
alternating from five (ten) primordials, and/or centrifugally.
Pollen grains tricolporate. Carpels five (although three also
frequent; when carpels two, then superposed). Style present.
Stigma not decurrent. Placentation axile. Endosperm development
nuclear. Fruit dry, dehiscent (when capsule then loculicidal).
RNase-based gametophytic incompatibility system present (stylar
response mediated by glycoprotein with RNase activity). Whole
genome triplication (γ triplication) leading to paleohexaploidy.
Cyanogenesis also via phenylalanine, isoleucine or valine
pathways (cyanogenic compounds also phenylalanine-, isoleucine-
or valine-derived). – Numerous stamens have evolved multiple
times in Pentapetalae. In these cases the stamens are
often arranged in fascicles. They may develop – centripetally or
centrifugally – from usually five antepetalous or ten separate
primordial or from an annular androecial primordium.

Synapomorphies other than
from DNA sequences have not been found for this clade. – The
position of Dilleniaceae
is still very unstable. They were recovered as sister-group to
the clade [Saxifragales+Rosidae]
(Superrosidae) in an analysis of complete plastid genome
sequence data (Moore & al. 2010). Presence of stipules
(usually inserted on the stem/branch) is a feature common to
Dilleniaceae
and rosids. On the other hand, in an analysis of inverted repeat
sequences, Dilleniaceae
were identified as sister to the clade
[Superasteridae+Superrosidae], i.e. to all
other Pentapetalae (Moore & al. 2011). In the
analyses by Soltis & al. (2011), Dilleniaceae
were sister-group to Superasteridae in the
maximum-likelihood analysis, whereas the maximum-parsimony
analysis revealed them as sister to Caryophyllales.
A position as sister to Caryophyllales
was revealed by Bell & al. (2010) and to
Superasteridae by Arakaki & al. (2011). Qiu &
al. (2010) recovered the topology [[Dilleniaceae+
Berberidopsidales]+[Asteridae+[Caryophyllales+Santalales]]].
Pending more convincing information I leave Dilleniaceae
as sister to Superasteridae, even if the support for the
position is not very strong.

Flowers
Actinomorphic or zygomorphic (rarely resupinate or asymmetrical).
Pedicel sometimes articulated. Hypogyny, epigyny or half epigyny.
Sepals (two to) four or five (to 16), with imbricate, valvate,
contorted or open aestivation, usually more or less connate.
Petals (three or) four or five (to 18), with imbricate, valvate,
contorted, convolute or ascending-cochlear (rarely induplicate,
descending-cochlear or open) aestivation, free from each other or
connate into campanulate, hypocrateromorphous, discoid,
urceolate, tubular or infundibuliform, often bilabiate corolla,
sometimes spurred. Nectaries usually present on petal bases or
intrastaminal nectariferous disc, usually annular (sometimes
cupular, rarely unilateral), entire or lobate, or as separate
nectariferous glands alternating with stamens, often only on
abaxial side (rarely absent).

Androecium
Stamens (two to) four or five (to 16, rarely to more than 1.200),
usually in one whorl, haplostemonous, antesepalous,
alternipetalous (rarely in two or several whorls). Filaments
usually free from each other (sometimes more or less connate),
usually adnate to petals/corolla tube (epipetalous). Anthers
usually free from each other (sometimes more or less connate,
occasionally adnate to style forming gynostegium), basifixed,
ventrifixed or dorsifixed, versatile or non-versatile, usually
tetrasporangiate (sometimes disporangiate or synthecal, rarely
monosporangiate or octosporangiate), usually extrorse or introrse
(rarely latrorse), usually longicidal (dehiscing by longitudinal
slits; rarely poricidal, dehiscing by apical or basal pores).
Placentoid often present. Tapetum secretory or
amoeboid-periplasmodial. Staminodia one to three or absent;
female flowers often with staminodia.

Fruit A
loculicidal and/or septicidal capsule (sometimes septifragal,
rarely a pyxidium, a denticidal capsule or irregularly
dehiscing), a drupe, a berry, an achene, or a schizocarp with
usually nutlike (rarely baccate, drupaceous or follicular)
mericarps (rarely a samara or syncarp).

Seeds Perisperm
not developed. Endosperm copious to sparse or absent, with
starch, oil, hemicellulose and/or proteins (sometimes with
petroselinic acid). Embryo straight to curved, sometimes oily,
well to poorly differentiated, usually without chlorophyll.
Cotyledons usually two (rarely one, four or absent), accumbent or
incumbent, rarely foliaceous.

Systematics The
combination of solitary and very long vessel elements (800 µm or
more) with scalariform perforation plates, usually opposite
pitting of vessel elements, non-septate and very long fibres
(2.190 µm or more) with bordered pits, and axial parenchyma
diffuse or diffuse-in-aggegates and paratracheal scanty (the
Baileyan wood anatomical syndrome) is abundant among asterids.
Compound leaves are fairly uncommon and the leaflets are often
articulated and/or distinct. Stipules are also relatively
infrequent.

Sympetalous zygomorphic flowers
are often combined with epipetalous stamens. Sympetaly is a
character common to the majority of Asteridae. Even many
clades with choripetalous flowers (possessing free petals) seem
to be principally sympetalous, since they develop an early
annular primordium and show early initiation of the corolla tube
(Leins & Erbar 2003; Erbar & Leins 2011). Early
initiation of the corolla tube occurs particularly among
Campanulidae (i.a. in Araliales,
Campanulales
and Dipsacales),
but also in some Lamiidae (e.g. Oleaceae
among Plantaginales,
and Rubiaceae
in Rubiales)
and in several Loasales.
Unfortunately, knowledge about corolla initiation in the basal
clades of Gentianidae is lacking.

The ovules in Asteridae
are usually characterized as tenuinucellar and unitegmic,
although the seemingly single integument may in fact be composed
of two fused integuments. In bitegmic asterids the outer
integument usually has a subdermal origin. The integument in
unitegmic asteroids are often dermal in origin and possibly
corresponds to the inner integument in most bitegmic
angiosperms.

Ellagic acid occurs
together with iridoids in many basal asterid clades, especially
in Loasales
and Ericales,
whereas ellagic acid is absent in Gentianidae. Moreover,
polyandry (possession of numerous stamens), a characteristic
feature of several clades in Loasales
and Ericales,
is very infrequent among Gentianidae (rare examples are
Hoplestigma in Boraginaceae
and Dialypetalanthus in Rubiaceae).
Polyandry may be correlated with increase in tepal (and sometimes
carpel) number, contrary to the case in non-asterid
Tricolpatae.

Synapomorphies other than
from DNA have not been found. – Garryales,
Icacinaceae,
Emmotaceae,
the Apodytes clade and Cassinopsis
form a basal grade in Garryidae. Oncotheca and
Metteniusa, formerly sometimes believed to be closely
allied to Garryales
or Icacinaceae,
form a basal grade (or perhaps clade) in Lamiidae. –
Garrya and Eucommia have only the d
copy of the gene RPB2, whereas RPB2 is
duplicated in Ilex.

Potential synapomorphies:
Carpels two, superposed. Introns 18–23 in d copy of gene
RPB2 lost. Caffeic acid present. – The I copy
of the gene RPB2 is present in most Lamiidae
and also in Ericales
(absent from Rosidae and remaining
Asteridae).

Scandianthus
costatus and S. major, from the Late Santonian to
the Early Campanian of southern Sweden, may be attributed to some
group of Lamiidae. They comprise bisexual actinomorphic
epigynous flowers with pentamerous perianth and androecium and a
gynoecium formed by two connate carpels. The sepals and petals
are free and the stamens diplostemonous. The nectariferous disc
is intrastaminal. The pollen grains are tricolporate and tectate,
the ovaries unilocular, the styles free, and the capsules
many-seeded and apically dehiscent.

Potential synapomorphies:
Nodes 1:1. Sepals connate. Anther theca with placentoid.
Endothelium present. Myricetin, iridoids and non-hydrolyzable
tannins usually absent. – Protein crystals seem to be frequently
present in the nucleus, although the knowledge of their
distribution is still very insufficient. Presence of arabino- and
galactoxyloglucans (instead of fucogalactoxyloglucans in cell
walls may be a synapomorphy.

Potential synapomorphies:
Vessel elements with scalariform perforation plates. Corolla with
valvate aestivation. Corolla tube initiation early; corolla tube
starting as annular meristem, ‘ring primordium’, from which
separate petals develop (petal primordia originating on ‘ring
primordium’ and staminal primordia arising in front of
interprimordial connections). Petals often with acuminate apex.
Endosperm copious. Embryo short or very short. Myricetin absent.
– Information on corolla tube initiation is very insufficient and
for numerous clades absent. Epigyny (inferior ovary) may be a
synapomorphy here, yet in that case with several reversals to
hypogyny. The I copy of the nuclear gene RPB2
is present in at least Escallonia of Escalloniaceae
and in Ilex (Aquifoliaceae),
but is lost in the majority of Campanulidae.
Ilex has also lost the introns 18–23 of the d
copy of RPB2, whereas these introns persist in
Escallonia. As usual, the situation in the smaller
clades (i.a. Bruniales
and Paracryphiales)
is not known.

Silvianthemum,
from the Late Santonian to the Early Campanian of southern
Sweden, comprises bisexual actinomorphic epigynous flowers with
pentamerous perianth and androecium and a gynoecium of three free
carpels. The surface is beset with peltate and simple hairs. The
eight or nine stamens are probably inserted in two series. The
pollen grains are tricolpate and tectate, the ovaries unilocular,
the styles free, and the numerous ovules anatropous and bitegmic.
A close relationship with Quintinia in Paracryphiaceae
has been suggested.

Flowers
Actinomorphic or zygomorphic (rarely asymmetrical). Pedicel often
articulated. Hypanthium sometimes present. Usually hypogyny
(sometimes epigyny or half epigyny). Receptacle sometimes
elongated into androgynophore or gynophore. Sepals (two to) four
to five (to c. 20), usually with imbricate or
imbricate-quincuncial, valvate or open (sometimes truncate,
contorted or decussate, rarely induplicate-valvate or cochlear)
aestivation, usually whorled (rarely [secondarily] spiral and
indistinctly separate from petals), usually free (sometimes
connate at base). Sepals often with three leaf traces from three
gaps. Petals (two to) four or five (to more than 15), usually
whorled (rarely spiral and indistinctly separate from sepals),
with imbricate or imbricate-quincuncial, valvate, contorted or
involute (sometimes crumpled, decussate or cochlear-descending,
rarely cochlear, plicate or open) aestivation, usually free
(sometimes more or less connate, rarely connate into campanulate
corolla), or absent. Nectaries receptacular, supplied from
receptacular or androecial traces, or on filament bases, or
staminodial, or extrastaminal or intrastaminal, annular, cupular,
unilateral or lobate, nectariferous disc, or as nectariferous
glands of various shape, inserted on disc, perianth, adaxial side
of hypanthium or as nectariferous hairs, or nectary absent. Disc
present or absent. Flower often with typical mucilage cells
having strongly thickened mucilaginous inner periclinal cell wall
and distinct cytoplasm.

Androecium
Stamens one to numerous (often 4+4 or 5+5; rarely more than
1.000), usually in one or more whorls, sometimes in three to five
alternisepalous or antesepalous fascicles, usually haplostemonous
or diplostemonous (sometimes obdiplostemonous, rarely
triplostemonous), centripetally or centrifugally developing.
Filaments free from each other or more or less connate, usually
free from tepals (sometimes adnate at base to petals,
epipetalous). Anthers basifixed or dorsifixed, versatile or
non-versatile, usually tetrasporangiate (rarely monosporangiate,
disporangiate or trisporangiate), usually introrse (sometimes
extrorse or latrorse), usually longicidal (dehiscing by
longitudinal slits; rarely poricidal, dehiscing by apical pores).
Tapetum usually secretory (rarely amoeboid-periplasmodial).
Staminodia present or absent.

Fruit A
loculicidal and/or septicidal (rarely septifragal or denticidal)
capsule, berry, drupe, nut, samara or schizocarp (divided into
two to five nut-like, samaroid, baccate or drupaceous mericarps;
rarely a pyxidium, a hesperidium, a secondary syncarp, or an
assemblage of achenes or follicles).

Seeds Perisperm
rarely developed. Endosperm copious to sparse, oily, sometimes
starchy, or absent. Embryo large or small, straight, plicate or
curved (rarely hook-shaped, spirally twisted or circinate),
usually well differentiated (rarely absent), oily, with or
without chlorophyll. Cotyledons usually two (rarely three or
four).

Fossils The
oldest known flower fossil showing rosid affinities (with
distinct calyx and corolla) emanate from the Late Albian to the
Early Cenomanian of Nebraska. This ‘Rose Creek flower’ is
pentamerous and hypogynous, with four series of floral parts,
free persistent sepals and free thin petals, probably five
antepetalous stamens, tricolporate pollen grains with psilate
exine, and five connate carpels with free styles.

Rosidae have
principally receptacular nectaries, whereas Vitaceae have
gynoecial nectaries. The corolla often has a delayed development
compared to other floral parts.

Phylogeny of Rosidae based on DNA
data (Wang & al. 2009; Worberg & al. 2009; Soltis
& al. 2011; somewhat modified). The bootstrap support
for Rosidae was 85% (Soltis & al. 2011), whereas the
support for the clades [Geraniales+Myrtales] and
[Cucurbitales+Juglandales] was 79% and 76%, respectively.
Vitaceae are sister to all other Rosidae (bootstrap
support 100%, although 72% in Wang & al. 2009).
Rosidae sensu stricto are split into the two clades
Fabidae (Zygophyllales to Juglandales) and Malvidae
(Myrtales to Capparales, BS support 97%). The branching
pattern within these clades are highly supported (75% to
100%). The support for the COM clade (Celastrales,
Oxalidales and Malpighiales) as sister to the
Nitrogen-fixing clade (Polygalales, Rosales, Cucurbitales
and Juglandales) was only 57%. The clade
[Malpighiales+Oxalidales], to which Celastrales are
sister-group, is supported by 59%. Zygophyllales may be
sister to [COM+Nitrogen-fixing-clade], but the support
for this is low. The COM clade is sister to Malvidae in a
study by Qiu & al. 2010.

Potential synapomorphies:
Extrafloral nectaries often consisting of palisade epidermal
cells. Endosperm scanty. – A trichotomy is formed by Zygophyllales,
the COM clade and the Nitrogen-fixing clade, or Zygophyllales
is sister-group to a clade comprising the COM and the
Nitrogen-fixing clades.

Symbiosis with
nitrogen-fixing Gram-positive actinobacteria, Frankia,
seems to have evolved at least four times (possibly six times).
The three lineages of Frankia have obviously diverged
prior to the origin of angiosperms. Frankia strains are
responsible for nitrogen-fixation in Cucurbitales
(i.a. Coriaria and Datisca), Juglandales
(e.g. Alnus, Casuarinaceae
and Myricaceae)
and Rosales (i.a.
Elaeagnaceae
and Rhamnaceae),
whereas N-fixation is carried out by Gram-negative
α-proteobacteria (Rhizobium) in Polygalales
(some Mimosoideae and the majority of Faboideae
inFabaceae)
and in Parasponia (Cannabaceae
in Rosales).
β-proteobacteria are responsible for the nodule formation and the
N-fixation in some Fabaceae
clades.

The underlying molecular
causes of developing nodular nitrogen-fixation are being explored
and it seems that plasmid-borne genetic components, which may be
exchanged between bacteria, are partly involved. Furthermore,
many genes directing the development of vesicular-arbuscular
mycorrhiza are identical to those involved in nodular N-fixation.
Ectomycorrhiza is frequently occurring among groups in the
Nitrogen-fixing clade. Nodulation probably involves interactions
between several genes.

The Frankia
nodules (and also the rhizobial nodules in Parasponia)
form through the modification of lateral roots, a process
directed by genes in the host plant. The pericyclic nodule
initiation results in the establishment of N-fixing bacterial
colonies in mid-cortical cells surrounding a central vascular
cylinder. The nodule tissues are enclosed by an outer periderm.
Intercellular penetration of root epidermis occurs in
Rosales
and may be a plesiomorphy, whereas in Cucurbitales
and Juglandales
the infection takes place via rhizoids (root hairs).

In Fabaceae
the nodules develop from root cortical cell divisions and their
vascular tissue becomes peripheral. The nodular initiation may
take place by intercellular penetration, infection through
rhizoids or infection at wound sites. The symbiosis between
Rhizobium and the plant is a prerequisite of the
nitrogen fixation, the fabaceous plant producing at least one of
the co-factor components essential for the nitrogenase activity.
The nitrogenase is present in Frankia in special
symbiotic vesicles located on short lateral branches of the
filamentous vegetative mycelium-forming bacterial cells. The
vesicles differ in their morphology among the lineages of the
Nitrogen-fixing clade (the NF clade).

Multiple parallel gains
and losses have probably taken place during the evolution of
nodular nitrogen-fixation among angiosperms. The majority of
groups included in the NF clade seem to lack the capacity of
forming root nodules and fix nitrogen. There may be a genetically
based predisposition with a single origin for nodular N-fixation
in the NF clade. If so, the common ancestor of the NF clade may
have evolved the underlying genetic requirements for bacterial
nodular N-fixation. Subsequently, parallel lineages would have
the necessary genetic equipment for developing N-fixing
mutualism. Alternatively, ancestors of many lineages in the NF
clade may have lost the ability to develop the symbiosis.

Although there is high
support for a single origin of nitrogen-fixing symbiosis, there
are significant differences in nodule morphology among the four
lineages of the NF clade. Apart from the rhizobial mutualism
carried out by Gram-negative proteobacteria in Fabaceae,
each of the remaining three (Frankia-inhabited) clades
exhibits a distinct nodule type.

In Rosaceae,
Elaeagnaceae
and Rhamnaceae
(Rosales) the
infection is carried out by hyphal penetration of the middle
lamella between epidermal cells of the root. Subsequent
intercellular bacterial growth takes place towards the cortex of
the root and, finally, penetration by the hyphae of cortical
cells in a nodule primordium.

Coriariaceae
and Datiscaceae
(Cucurbitales)
are infected via rhizoids (root hairs). They also have a specific
arrangement of vesicles in infected cells, with vesicles
orientated at right angles to a central vacuole instead of
vesicles surrounding the periphery of the cytoplasm.
Coriaria and Datisca possess well-aerated
nodule tissue and their nodules have a specific cell layer that
limits the diffusion of oxygen. Datisca produces nodule
roots, as is the case in Myricaceae
(Juglandales),
whereas Coriaria does not produce nodule roots. Instead,
Coriaria has lenticels, through which oxygen may pass
into the nodule. Moreover, the non-infected cells are separate
from the multinucleate infected cells.

The nodules of
Casuarinaceae
and Myricaceae
(Juglandales)
possess a specialized cell layer which has thick or lignified
walls and is resistant against oxygen diffusion, resulting in a
lower oxygen concentration in the Frankia-infected
cells. The growth of the nodule lobes (formation of the nodular
roots) in Juglandales
is usually indeterminate. This probably results in higher
absorption of oxygen due to the increased surface area.
Alnus, which does not produce nodule roots, is an
exception to this. Instead, Alnus (having well-aerated
nodule tissue) possesses nodule lenticels, which are similar to
those in Coriaria (Cucurbitales)
and enhance the transport of free oxygen into the nodules (oxygen
diffusion resistance layer is absent in Alnus).
Furthermore, the haemoglobin concentration is usually higher in
the nodules of Juglandales
(again, Alnus is an exception).

Potential synapomorphies:
Placentation apical. Ovules two per carpel, pendulous. – This
clade is sister to Staphyleales.

The relationships in
Malvidae are unclear and it is not at all certain which
group is sister to Capparales.
The clade [Malvales+Sapindales]
is a possible candidate, and the clade [Malvales+Capparales]
has large support in some analyses, although the sampling was
insufficient and Huerteales
was not included.

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